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One of two tandem Arabidopsis genes homologous to monosaccharide transporters is senescence-associated

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Abstract

A gene designated SFP1, which is similar to major facilitator superfamily monosaccharide transporters, is induced during leaf senescence. Genomic sequence analysis identified a second highly similar and closely linked gene, SFP2, suggesting that SFP1 and SFP2 may have arisen through a recent duplication event. However, RNA gel-blot analyses and histochemical localization of a reporter gene activity in transgenic plants show that SFP1 and SFP2 are differentially regulated and that only SFP1 is induced during leaf senescence. The increase in SFP1 gene expression during leaf senescence is paralleled by an accumulation of monosaccharides. Possible roles for SFP1 in sugar transport during leaf senescence are discussed.

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References

  • An, Y.Q., Huang, S., McDowell, J.M., McKinney, E.C. and Meagher, R.B. 1996. Conserved expression of Arabidopsis ACT1 and ACT3 actin subclass in organ primordia and mature pollen. Plant Cell 8: 15–30.

    Google Scholar 

  • Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815.

    Google Scholar 

  • Bechtold, N. and Pelletier, G. 1998. In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plant by vacuum infiltration. Meth. Mol. Biol. 82: 259–266.

    Google Scholar 

  • Benner, J.L. and Noodén, L.D. 1984. Translocation of photo-synthate from soybean leaves to the pods during senescence. Biochem. Physiol. Pflanzen 179: 269–275.

    Google Scholar 

  • Bleecker, A.B. and Patterson, S.E. 1997. Last exit: senescence, abscission, and meristem arrest in Arabidopsis. Plant Cell 9: 1169–1179.

    Google Scholar 

  • Boorer, K.J., Loo, D.D. and Wright, E.M. 1994. Steady-state and presteady-state kinetics of the H +/hexose cotransporter (STP1) from Arabidopsis thaliana expressed in Xenopus oocytes. J. Biol. Chem. 269: 20417–20424.

    Google Scholar 

  • Buttner, M. and Sauer, N. 2000. Monosaccharide transporters in plants: structure, function and physiology. Biochim. Biophys. Acta 1465: 263–274.

    Google Scholar 

  • Buttner, M., Truernit, E., Baier, K., Scholz-Starke, J., Sontheim, M., Lauterbach, C., Huss, V.A.R. and Sauer, N. 2000. AtSTP3, a green leaf-specific, low affinity monosaccharide-H +symporter of Arabidopsis thaliana. Plant Cell Envir. 23: 175–184.

    Google Scholar 

  • Chiou, T.J. and Bush, D.R. 1996. Molecular cloning, immunochemical localization to the vacuole, and expression in transgenic yeast and tobacco of a putative sugar transporter from sugar beet. Plant Physiol. 110: 511–520.

    Google Scholar 

  • Crafts-Brandner, S.J., Below, F.E., Wittenbach, V.A., Harper, J.E. and Hageman, R.H. 1984. Differential senescence of maize hy-brids following ear removal. II. Selected leaf. Plant Physiol. 74: 368–373.

    Google Scholar 

  • Dunphy, E.J. and Hanway, J.J. 1976. Water-soluble carbohydrate accumulation in soybean plants. Agron. J. 68: 697–700.

    Google Scholar 

  • Ehlers, K. and van Bel, A.J.E. 1999. The physiological and developmental consequences of plasmodesmatal connectivity. In: A.J.E. van Bel and W.J.P. van Kesteren (Eds.) Plamadesmata: Structure, Function, Role in Cell Communication, Springer-Verlag, Heidelberg, Germany, pp. 243–260.

    Google Scholar 

  • Getz, H., Knauer, D. and Willenbrink, J. 1987. Transport of sugars across the plasma membrane of beet root protoplasts. Planta 171:185–196.

    Google Scholar 

  • Gogarten, J.P. and Bentrup, F. 1989. Substrate specificity of the hexose carrier in the plasmalemma of Chenopodium suspension cells probed by transmembrane exchange diffusion. Planta 178: 52–60.

    Google Scholar 

  • Griffith, J.K., Baker, M.E., Rouch, D.A., Page, M.G., Skurray, R.A., Paulsen, I.T., Chater, K.F., Baldwin, S.A. and Henderson, P.J. 1992. Membrane transport proteins: implications of sequence comparisons. Curr. Opin. Cell Biol. 4: 684–695.

    Google Scholar 

  • Hajdukiewicz, P., Svab, Z. and Maliga, P. 1994. The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25: 989–994.

    Google Scholar 

  • Harrison, M.J. 1996. A sugar transporter from Medicago tuncatula: altered expression pattern in roots during vesicular-arbuscular (VA) mycorrhizal associations. Plant J. 9: 491–503.

    Google Scholar 

  • Hnesel, L.L., Grbic, V., Baumgarten, D.A. and Bleecker, A.B. 1993. Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in Ara-bidopsis. Plant Cell 5: 553–564.

    Google Scholar 

  • Kyte, J. and Doolittle, R.F. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157: 105–132.

    Google Scholar 

  • Lalonde, S., Boles, E., Hellman, H., Barker, L., Patrick, J.W., From-mer, W.B. and Ward, J.M. 1999. The dual functions of sugar carriers. Transport and sugar sensing. Plant Cell 11: 707–726.

    Google Scholar 

  • Lohman, K., Gan, S., John, M. and Amasino, R.M. 1994. Molecular analysis of natural leaf senescence in Arabidopsis thaliana.Physiol. Plant. 92: 322–328.

    Google Scholar 

  • Maynard, J.W. and Lucas, W.J. 1982. Sucrose and glucose uptake into Beta vulgaris leaf tissues. Plant Physiol. 70: 1436–1443.

    Google Scholar 

  • Murashige, T. and Skoog, F. 1962. A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol. Plant. 15: 473–497.

    Google Scholar 

  • Noodén, L.D. 1988. The phenomena of senescence and aging. In:L.D. Noodén and A.C. Leopold (Eds.) Senescence and Aging in Plants, Academic Press, San Diego, CA, pp. 1–50.

    Google Scholar 

  • Pao, S.S., Paulsen, I.T. and Saier Jr., M.H. 1998. Major facilitator superfamily. Microbiol. Mol. Biol. Rev. 62: 1–34.

    Google Scholar 

  • Peoples, M.B., Beilharz, V.C., Waters, S.P., Simpson, R.J. and Dalling, M.J. 1980. Nitrogen redistribution during grain growth in wheat (Tritcum aestivum L.). Planta 149: 241–251.

    Google Scholar 

  • Quirino, B.F., Normanly, J. and Amasino, R.M. 1999. Diverse range of gene activity during Arabidopsis thaliana leaf senescence includes pathogen-independent induction of defense-related genes. Plant Mol. Biol. 40: 267–278.

    Google Scholar 

  • Quirino, B.F., Noh, Y.-S., Himelblau, E. and Amasino, R.M. 2000.Molecular aspects of leaf senescence. Trends Plant Sci. 5: 278–282.

    Google Scholar 

  • Reckmann, U., Scheibe, R. and Raschke, K. 1990. Rubisco activity in guard cells compared with the solute requirement for stomatal opening. Plant Physiol. 92: 246–253.

    Google Scholar 

  • Reiter, W.D., Chapple, C.C.S. and Somerville, C.R. 1993. Altered growth and cell walls in a fucose-deficient mutant of Arabidopsis. Science 261: 1032–1035.

    Google Scholar 

  • Roitsch, T. and Tanner, W. 1994. Expression of a sugar-transporter gene family in a photoautotrophic suspension culture of Chenopodium rubrum L. Planta 193: 365–371.

    Google Scholar 

  • Sauer, N. and Stolz, J. 1994. SUC1 and SUC2: two sucrose transporters from Arabidopsis thaliana; expression and characterization in baker's yeast and identification of the histidine-tagged protein. Plant J. 6: 67–77.

    Google Scholar 

  • Sauer, N., Friendlander, K. and Graml-Wicke, U. 1990. Primary structure, genomic organization and heterologous expression of a glucose transporter from Arabidopsis thaliana.EMBOJ.9: 3045–3050.

    Google Scholar 

  • Sauer, N. Baier, K., Gahrtz, M., Stadler, R., Stolz, J and Truernit, E. 1994. Sugar transport across the plasma membranes of higher plants. Plant Mol. Biol. 26: 1671–1679.

    Google Scholar 

  • Smart, C.M. 1994. Tansley Review No. 64. Gene expression during leaf senescence. New Phytol. 126: 419–448.

    Google Scholar 

  • Thomson, W.W. and Platt-Aloia, K.A. 1987. Ultrastructural changes associated with senescence. In: W.W. Thomson, E.A. Nothnagel and R.C. Huffaker (Eds.) Plant Senescence: Its Biochemistry and Physiology,American Society of Plant Physiology, Rockville,MN, pp. 20–30.

    Google Scholar 

  • Truernit, E., Schmid, J., Epple, P., Illig, J. and Sauer, N. 1996. The sink-specific and stress-regulated Arabidopsis STP4 gene: enhanced expression of a gene encoding a monosaccharide trans-porter by wounding, elicitors, and pathogen challenge. Plant Cell 8: 2169–2182.457

    Google Scholar 

  • Truernit, E., Stadler, R., Baier, K. and Sauer, N. 1999. A male gametophyte-specific monosaccharide transporter in Arabidop-sis. Plant J. 17: 191–201.

    Google Scholar 

  • Tubbe, A. and Buckhout, T.J. 1992. In vitro analysis of the H +-hexose symporter on the plasma membrane of sugar beets (Beta vulgaris L.). Plant Physiol. 99: 945–951.

    Google Scholar 

  • Weaver, L.M., Himelblau, E. and Amasino, R.M. 1997. Leaf senescence: gene expression and regulation. Genet. Eng. 19: 215–234.

    Google Scholar 

  • Weaver, L.M., Gan, S., Quirino, B. and Amasino, R.M. 1998. A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol. Biol. 37: 455–469.

    Google Scholar 

  • Weber, H., Borisjuk, L., Heim, U., Sauer, N. and Wobus, U. 1997.A role for sugar transporters during seed development: molecular characterization of a hexose and a sucrose carrier in fava bean seeds. Plant Cell 9: 895–908.

    Google Scholar 

  • Weig, A., Franz, J., Sauer, N. and Komor, E. 1994. Isolation of a family of cDNA clones from Ricinus communis L. with close homology to the hexose carriers. J. Plant Physiol. 143: 178–183.

    Google Scholar 

  • Wingler, A., Schaewen, A., Leegood, R.C., Lea, P.J. and Quick, W.P. 1998. Regulation of leaf senescence by cytokinins, sugars, and light. Plant Physiol. 116: 329–335.

    Google Scholar 

  • Wintermans, J.F.G.M. and DeMots, A. 1965. Spectrophotometric characteristics of chlorophylls a and b and their pheophytins in ethanol. Biochim. Biophys. Acta 109: 448–453.

    Google Scholar 

  • Ylstra, B., Garrido, D., Busscher, J. and van Tunen, A.J. 1998. Hexose transport in growing petunia pollen tubes and characterization of a pollen-specific, putative monosaccharide transporter. Plant Physiol. 118: 297–304.

    Google Scholar 

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Quirino, B.F., Reiter, WD. & Amasino, R.D. One of two tandem Arabidopsis genes homologous to monosaccharide transporters is senescence-associated. Plant Mol Biol 46, 447–457 (2001). https://doi.org/10.1023/A:1010639015959

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